Melinda A. Fowler

Foraging Behavior and Success of a Mesopelagic Predator in the Northeast Pacific Ocean: Insights from a Data-Rich Species, the Northern Elephant Seal

The mesopelagic zone of the northeast Pacific Ocean is an important foraging habitat for many predators, yet few studies have addressed the factors driving basin-scale predator distributions or inter-annual variability in foraging and breeding success. Understanding these processes is critical to reveal how conditions at sea cascade to population-level effects. To begin addressing these challenging questions, we collected diving, tracking, foraging success, and natality data for 297 adult female northern elephant seal migrations from 2004 to 2010. During the longer post-molting migration, individual energy gain rates were significant predictors of pregnancy. At sea, seals focused their foraging effort along a narrow band corresponding to the boundary between the sub-arctic and sub-tropical gyres. In contrast to shallow-diving predators, elephant seals target the gyre-gyre boundary throughout the year rather than follow the southward winter migration of surface features, such as the Transition Zone Chlorophyll Front. We also assessed the impact of added transit costs by studying seals at a colony near the southern extent of the species’ range, 1,150 km to the south. A much larger proportion of seals foraged locally, implying plasticity in foraging strategies and possibly prey type. While these findings are derived from a single species, the results may provide insight to the foraging patterns of many other meso-pelagic predators in the northeast Pacific Ocean.

Fasting Physiology of the Pinnipeds: The Challenges of Fasting While Maintaining High Energy Expenditure and Nutrient Delivery for Lactation

Most animal species experience periods of food deprivation and many periodically forgo foraging in favor of other activities such as migration and reproduction. Pinnipeds—seals, sea lions, fur seals, and walrus—forage on marine resources but remain tied to land for reproduction. This separates energy acquisition from energy allocation for maternal investment, competition for mates, and for tissue maintenance and repair during pelage synthesis. Thus, pinnipeds regularly undertake energetically costly activities simultaneous with extended fasting at multiple life stages. This life history characteristic should favor physiological mechanisms for efficient fasting metabolism while supporting the energetic and substrate requirements of energy-demanding activities (e.g. lactation). Studies on a variety of pinnipeds have revealed highly efficient protein sparing despite high rates of energy expenditure and nutrient mobilization for lactation. Carbohydrate oxidation is low and high rates of lipolysis support nutrient delivery. Despite prolonged fasting and high rates of β-oxidation there is little accumulation of ketoacids. In contrast to numerous investigations on nonfasting adapted species, studies on phocid seals have revealed high rates of glucose production during fasting that exceed the needs for glucose dependent tissues and suggest high rates of carbohydrate recycling. Investigations into the hormonal regulation of fuel use and intracellular signaling pathways indicate adjustments to the typical mammalian regulation of gluconeogenesis. Together, these findings suggest alterations in the metabolic strategies for fasting exist in the pinnipeds compared to domestic and wild terrestrial mammals.

Gluconeogenesis is associated with high rates of tricarboxylic acid and pyruvate cycling in fasting northern elephant seals

Animals that endure prolonged periods of food deprivation preserve vital organ function by sparing protein from catabolism. Much of this protein sparing is achieved by reducing metabolic rate and suppressing gluconeogenesis while fasting. Northern elephant seals (Mirounga angustirostris) endure prolonged fasts of up to 3 mo at multiple life stages. During these fasts, elephant seals maintain high levels of activity and energy expenditure associated with breeding, reproduction, lactation, and development while maintaining rates of glucose production typical of a postabsorptive mammal. Therefore, we investigated how fasting elephant seals meet the requirements of glucose-dependent tissues while suppressing protein catabolism by measuring the contribution of glycogenolysis, glycerol, and phosphoenolpyruvate (PEP) to endogenous glucose production (EGP) during their natural 2-mo postweaning fast. Additionally, pathway flux rates associated with the tricarboxylic acid (TCA) cycle were measured specifically, flux through phosphoenolpyruvate carboxykinase (PEPCK) and pyruvate cycling. The rate of glucose production decreased during the fast (F(1,13) = 5.7, P = 0.04) but remained similar to that of postabsorptive mammals. The fractional contributions of glycogen, glycerol, and PEP did not change with fasting; PEP was the primary gluconeogenic precursor and accounted for ∼95% of EGP. This large contribution of PEP to glucose production occurred without substantial protein loss. Fluxes through the TCA cycle, PEPCK, and pyruvate cycling were higher than reported in other species and were the most energetically costly component of hepatic carbohydrate metabolism. The active pyruvate recycling fluxes detected in elephant seals may serve to rectify gluconeogeneic PEP production during restricted anaplerotic inflow in these fasting-adapted animals.

Adiposity and Fat Metabolism in Lactating and Fasting Northern Elephant Seals

Several taxa of animals fast completely from food and water during energy-intensive periods such as lactation, breeding, and development. In elephant seals, these behaviors are sustained by high adiposity, high rates of fat mobilization, and reduced oxidation of carbohydrates and proteins. Adiposity and the regulation of lipolysis directly affect lactation energetics, milk composition, and mating success. Long-term fasting induces changes in regulation of lipolysis and lipid metabolism that influence fatty acid (FA) availability and the onset of insulin resistance. Hypoinsulinemia and elevated circulating FAs are also associated with several unique features of carbohydrate metabolism, including elevated plasma glucose, gluconeogenesis, and Cori cycle activity as well as high rates of pyruvate and tricarboxylic acid cycling. Glucose-lactate pools and triacylglycerol-FA cycles may be linked via glyceroneogenesis and this may be an important pathway influencing both fat and carbohydrate metabolism. Together, these features allow a sustained, high intensity, fat-based metabolism without substantial accumulation of ketoacids.

Mobile receivers: releasing the mooring to ‘see’ where fish go

Much has been learned from the large scale deployment of acoustic tags on aquatic species and associated networks of riverine and marine receivers. While effective in the linear environment of river systems, marine systems limit the ability to provide spatial information on fish movements and distributions due to a combination of costs, logistics, and lack of off-shore technology. At the same time, each year millions of dollars worth of tags are being released into the aquatic environment with extended battery/transmission life, yet detections are limited to coastal arrays. Here we explore new methods of tracking acoustically tagged species in the marine environment. A new miniaturized acoustic receiver, the Vemco Mobile Transceiver (VMT) can be carried by large marine organisms. In combination with satellite and archival tag technology, VMTs were deployed on northern elephant seals to monitor acoustic tags encountered during their migrations across the Northeast Pacific. Early results include acoustic detections of tagged great white sharks, salmon sharks, Chinook salmon, steelhead, lingcod, green sturgeon and other elephant seals. We also propose several alternative directions for future effort: 1) analyzing the growing number of passive acoustic survey recordings made from hydrophone arrays for acoustic tag detections, 2) working with acoustic technology providers to develop hull-mounted receiver systems for the thousands of ocean going vessels around the world and 3) integrating acoustic receiver technology into the thousands of moored and drifting oceanographic buoy arrays.

Differential changes of fat-soluble vitamins and pollutants during lactation in northern elephant seal mother-pup pairs.

We investigated the changes of vitamins A and E as well as PCBs and DDTs during lactation in northern elephant seal (Mirounga angustirostris) mother-pup pairs. On average, milk vitamin A concentrations were 6 times higher during late lactation than during early lactation, a pattern that differs dramatically from terrestrial mammals. Vitamin A concentrations also significantly increased in the inner blubber throughout lactation, whereas they remained constant in the outer blubber. Similar dynamics were observed for PCBs and DDTs in maternal blubber and milk. Blubber appears to be an important storage site for vitamin A and organochlorines in seals and a direct transfer of those molecules to the mammary gland may occur. The dynamics of vitamin A, PCBs and DDTs differed from those of vitamin E. There was a significant drop in milk vitamin E concentrations between early and late lactation, which is the usual pattern observed in terrestrial mammals. The dynamics of vitamin E in the blubber layers also differed from those of vitamin A, suggesting different mechanisms of mobilization and transfer into the milk.

A profile of carbohydrate metabolites in the fasting northern elephant seal

Northern elephant seals endure prolonged periods of food deprivation at multiple life-history stages and simultaneous with energetically costly activities-including reproduction and development. Most mammals decrease their energy expenditure while fasting, with simultaneous reductions in gluconeogenesis and circulating glucose concentration. Paradoxically, elephant seals maintain high rates of both energy expenditure and gluconeogenesis, and high blood glucose concentrations throughout fasting. We therefore characterized the suite of changes that occur in carbohydrate metabolites during fasting in northern elephant seals. Using a broad-based metabolomics platform we investigated fasting during two states-lactation in adult females and the post-weaning developmental period in pups. A total of 227 metabolites were detected in seal plasma; 31 associated with carbohydrate metabolism were analyzed in the present study. Several compounds showed similar responses during lactation and the post-weaning fast (e.g. glycerol and mesaconate) whereas other compounds displayed quite different abundances between groups (e.g. citrate and pyruvate). This work found that, while the changes that occur with fasting were frequently similar in lactating females and developing pups, the relative abundance of compounds often varied markedly. These differences suggest that the metabolic strategies used to endure prolonged fasts are influenced by life-history or nutrient constraints.

Mid-winter temperatures, not spring temperatures, predict breeding phenology in the European starling Sturnus vulgaris.

In many species, empirical data suggest that temperatures less than 1 month before breeding strongly influence laying date, consistent with predictions that short lag times between cue and response are more reliable, decreasing the chance of mismatch with prey. Here we show in European starlings (Sturnus vulgaris) that mid-winter temperature ca 50–90 days before laying (8 January–22 February) strongly (r2 = 0.89) predicts annual variation in laying date. Mid-winter temperature also correlated highly with relative clutch size: birds laid later, but laid larger clutches, in years when mid-winter temperatures were lower. Despite a high degree of breeding synchrony (mean laying date 5–13 April = ±4 days; 80% of nests laid within 4.8 days within year), European starlings show strong date-dependent variation in clutch size and productivity, but this appears to be mediated by a different temporal mechanism for integration of supplemental cue (temperature) information. We suggest the relationship between mid-winter temperature and breeding phenology might be indirect with both components correlating with a third factor: temperature-dependent development of the starlings insect (tipulid) prey. Mid-winter temperatures might set the trajectory of growth and final biomass of tipulid larvae, with this temperature cue providing starlings with information on breeding season prey availability (though exactly how remains unknown).

Individual variation in workload during parental care: can we detect a physiological signature of quality or cost of reproduction?

How hard do birds work during parental care, chick rearing, or provisioning of their nestlings? And if birds do work hard, can we detect a physiological signature of individual variation in workload ability (perhaps related to ‘quality’) or costs associated with high workload? Here, we provide a broad conceptual perspective on these questions. Life-history theory predicts (or requires) that (1) parental care is hard work, (2) individuals that invest more in parental care benefit in terms of rearing more, larger, fitter offspring, but that (3) increased investment in parental care comes at a cost: decreased future fecundity and/or survival. However, we start by highlighting studies that are inconsistent with this conventional view, e.g., (1) females often do not pay a survival cost of increased workload (though males do), (2) some (high quality?) individuals appear to maximise numerous life-history traits, and (3) workload during parental care often does not predict productivity. We suggest that an “exercise physiology” perspective on parental care might be informative, but highlight the fact that existing models of exercise often involve conditions very different from that free-living animals experience while foraging (e.g., using forced exercise) and are often divorced from the critical relationship in free-living animals between exercise and acquisition of resources. We briefly review studies looking at physiological effects of workload during parental care in free-living birds, but again highlight our surprising lack of knowledge in this area especially where experimental manipulation of workload is coupled with comprehensive, physiological analysis. Finally, we make three recommendations for how can we advance the study of physiology of parental care in chick-rearing birds: (1) experimental manipulation of workload, (2) obtaining better measures of workload, for large numbers of known-individuals, and (3) better assessment of physiology of individual quality, and identification of specific metrics of workload-induced ‘wear and tear’.

Metabolic response to a glucagon challenge varies with adiposity and life-history stage in fasting northern elephant seals

Metabolic adaptations for extended fasting in wildlife prioritize beta-oxidation of lipids and reduced glucose utilization to support energy metabolism. The pancreatic hormone glucagon plays key roles in regulating glycemia and lipid metabolism during fasting in model species but its function in wildlife species adapted for extended fasting is not well understood. Northern elephant seals (NES) undergo natural fasts of 1-3months while under constraints of high nutrient demands including lactation and development. We performed a glucagon challenge on lactating, molting and developing NES, early and late in their natural fasts, to examine the impact of this important regulatory hormone on metabolism. Glucagon caused increases in plasma glucose, insulin, fatty acids, ketones and urea, but the magnitude of these effects varied widely with adiposity and life-history stage. The strong impact of adiposity on glucose and insulin responses suggest a potential role for adipose derived factors in regulating hepatic metabolism and pancreatic sensitivity. Elevations in plasma glucose in response to glucagon were strongly associated with increases in protein catabolism, suggesting negative impacts of elevated glucagon on protein sparing. Glucagon promoted rapid ketone accumulation suggesting that low ketoacid levels in NES reflect low rates of production. These results demonstrate strong metabolic impacts of glucagon and support the idea that glucagon levels are downregulated in the context of metabolic adaptation to extended fasting. These results suggest that the regulation of carbohydrate and lipid metabolism in NES changes with adiposity, fasting duration and under various constraints of nutrient demands.